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Article Assessment of Quality, , and in Burullus,

Ahmed E. Alprol 1, Ahmed M. M. Heneash 1, Asgad M. Soliman 1, Mohamed Ashour 1,* , Walaa F. Alsanie 2, Ahmed Gaber 3 and Abdallah Tageldein Mansour 4,5

1 National Institute of and , NIOF, 11516, Egypt; [email protected] (A.E.A.); [email protected] (A.M.M.H.); [email protected] (A.M.S.) 2 Department of Clinical Laboratories , The Faculty of Applied Medical Sciences, Taif University, P.O. Box 11099, Taif 21944, Saudi Arabia; [email protected] 3 Department of , College of , Taif University, P.O. Box 11099, Taif 21944, Saudi Arabia; [email protected] 4 and Production Department, College of Agricultural and Food Sciences, King Faisal University, P.O. Box 420, Al-Ahsa 31982, Saudi Arabia; [email protected] 5 Fish and Animal Production Department, Faculty of (Saba Basha), University, Alexandria 21531, Egypt * Correspondence: [email protected]

Abstract: Burullus Lake is Egypt’s second most important coastal . The present study aimed to shed on the different types of polluted entering the lake from various drains, as well

 as to evaluate the zooplankton community, determine the physical and chemical characteristics of  the waters, and study the eutrophication state based on three years of seasonal monitoring from

Citation: Alprol, A.E.; Heneash, 2017 to 2019 at 12 stations. The results revealed that Rotifera, Copepoda, , and A.M.M. ; Soliman, A.M.; Ashour, M.; dominated the zooplankton population across the three-year study period, with a total of 98 taxa from Alsanie, W.F.; Gaber, A.; Mansour, 59 genera and 10 groups detected in the whole-body lake in 2018 and 2019, compared to 93 A.T. Assessment of , from 52 genera in 2017. Twelve representative samples were collected from the lake to Eutrophication, and Zooplankton determine physicochemical parameters, i.e., temperature, pH, salinity, dissolved , biological Community in Lake Burullus, Egypt. oxygen demand, chemical oxygen demand, -N, –N, nitrate-N, total , total Diversity 2021, 13, 268. https:// , dissolved reactive phosphorus, and chlorophyll-a, as well as Fe, Cu, Zn, Cr, Ni, Cd, doi.org/10.3390/d13060268 and Pb ions. Based on the calculations of the water quality index (WQI), the lake was classified as having good water quality. However, the trophic state is ranked as hyper-eutrophic and high trophic Academic Editors: Boris A. Levin and conditions. Yulia V. Bespalaya

Keywords: zooplankton community; marine ; water quality; eutrophication state; heavy Received: 29 April 2021 Accepted: 11 June 2021 metals; Burullus Lake Published: 15 June 2021

Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in 1. Introduction published maps and institutional affil- The Deltaic Mediterranean coastline of Egypt, especially the middle part, has economic iations. importance. From the west to the east coast, there are three Deltaic shallow (Edku, Burullus, and Manzala Lakes). Burullus Lake is the second-largest natural lake in Egypt and is situated close to the Mediterranean among the two main branches of the Nile. The importance of lakes as natural resources includes fish production, as they account Copyright: © 2021 by the authors. for more than 40% of the overall fish production in Egypt. As a result of anthropogenic Licensee MDPI, Basel, Switzerland. activity and pollution, its production has decreased to less than 12.22% now [1]. Burullus This article is an open access article Lake is one of a network of protected areas throughout Egypt, designated and managed distributed under the terms and by the Egyptian Environmental Affairs Agency. It is registered as a in 1998. conditions of the Creative Commons Additionally, Birdlife International has identified it as an important bird area (IBA) [2], due Attribution (CC BY) license (https:// to its importance for , migratory , and breeding of water birds [3]. It covers creativecommons.org/licenses/by/ an area of 410 km2 [4] of which 220 km2 are open water [5]. It is observable that the open 4.0/).

Diversity 2021, 13, 268. https://doi.org/10.3390/d13060268 https://www.mdpi.com/journal/diversity Diversity 2021, 13, 268 2 of 23

water surface in the lake had reduced from 1092 km2 in 1801 [6] to 434.6 km2 in 1972 then reduced to 220 km2 in 2015 with a reduction of about 80.0% of the water area [5]. Coastal lakes are heavily influenced by anthropogenic activities from watersheds, as they receive inputs of freshwater and polluted waters containing organic and inorganic compounds from different sources [7]. These lakes collect massive amounts of drainage water from various drains around the Nile delta and connect to the via El-Boughaz outlets [2]. Contamination of the marine environment is a major factor that poses a substantial threat to marine creatures’ survival [8]. Among the several , are toxic, persistent, and abundant owing to their accumulation in the and continued persistence in the and their concentration increases through biomagnification [9]. The impacts of pollution have far-reaching consequences for public health, the economy, and the environment [10]. The process of eutrophication is driven by an increase in in the aquatic systems, particularly nitrogen and phosphorus in the ecosystem, which leads to an increase in () and an accumulation of organic matter in the lakes. In addition, silt from the drainage basins will accumulate over time, which makes the lake shallower and warmer. Eutrophication can also have a negative impact on the as well as the natural stability of the lake, affecting practically all of the biological communities and their interactions in the water body [11]. Under natural conditions, the rate of this process is very slow and it takes hundreds or thousands of years. Zooplankton are aquatic species with poor swimming abilities that float in the of , , or freshwater bodies to travel for long distances [8,12,13]. Zooplank- tons are important in the ecosystem because they connect the primary production and the higher levels, monitoring water quality, pollution, and the state of eutrophication [14,15]. In addition, zooplankton play an important role in the natural cycle of and other elements in the sea [16]. On the other hand, zooplankton are the main suitable feeds for larval stages of many fish and shellfish species in marine hatcheries [8,12]. Seasonal zooplankton movement and the factors driving their inconstancy are very sensitive to changes in ecological variables, particularly in shallow, semi-enclosed inlets with densely populated shores, where increasing anthropogenic input has a serious influence on marine communities [17,18]. Monitoring of water quality is the first step that can lead to management and conservation of aquatic . The chemical and physical factors influencing the marine environment include temperature, pH, salinity, dissolved oxygen, biological oxygen demand, chemical oxygen demand, nutrients, reactive , heavy metal pollutants, and others. These parameters are considered the most limiting factors affecting the survival and growth of aquatic [19–21]. Poor water quality could be produced via low aquatic flow, municipal discharges, and wastewater effluents [22]. In this study, Burullus Lake was chosen because of its economic importance in Egypt, based on its various uses and surroundings, such as tourism, fisheries activity, nutrient enrichment, and industrial water sources, among others. Furthermore, any noticeable change in water quality has an impact on the health, structure, and growth of the fish population, so this paper aims to determine most of the parameters related to water quality and identify the major sources of pollution in Burullus Lake, Egypt over the course of three years, from 2017–2019, in conjunction with the study of eutrophication state and an assessment of potential ecological concerns. In addition, it aims to assess the community, occurrence, diversity, and of zooplankton in Burullus Lake. Moreover, the current study will be a useful tool in assisting decision makers and authorities in charge for sustainable marine management and increasing the lake production.

2. Materials and Methods 2.1. Study Area and Sampling Burullus Lake is located at (30◦220–31◦350 N; 30◦330–31◦080 E) with an area of about 460 km2, length of about 47 km, and width ranges between 6 and 16 km. It has an irregular elongated shape with 0.4–2.5 m depth. The lake receives through a long canal Diversity 2021, 13, 268 3 of 23

(Boughaz El-Burullus) that connects the lake to the sea. enters the lake through 8 drains and 1 freshwater canal. The lake is divided into 3 basins; eastern, middle, and western. It is situated on the eastern port of side of the Nile. Water samples were collected seasonally for the period from winter 2017 to autumn 2019 in sterile containers and maintained in an icebox on the site. A total of 12 surface water samples were collected from 12 sites representing different environmental . Information of the sampling sites with their latitude and longitude are presented in Table1 and Figure1.

2.2. Methods Analyses of the physicochemical parameters of collected water samples were in- vestigated according to the standard methods APHA [23] to estimate various factors, such as biological oxygen demand (BOD), chemical oxygen demand (COD), ammonia-N, nitrate–N, nitrate-N, total nitrogen, dissolved reactive phosphorus, total phosphorus, and chlorophyll-a (Chlo-a). Water temperature was determined by a thermometer. The concentration of hydrogen ion (pH) was determined by pH meter Model 59003-20 USA. Salinity (‰) was measured by the Cole–Parmer model Check-mate 90 (CORNING) conductivity meter. Dissolved oxygen (DO) was measured by using the modified Winkler method.

2.2.1. Determination of Heavy Metals in Water Water samples were filtered by 0.45 µm membrane filters. The filtrate water samples were preconcentrated individually with pyrrolidine di-thiocarbamate (APDC)- methyl isobutyl ketone (MIBK) extraction procedure APHA [23]. The Fe, Cu, Zn, Cr, Ni, Cd, and Pb were determined by atomic absorption spectrometer according to standard methods.

2.2.2. Zooplankton Quantitative Analysis A horizontal quantitative sample was taken at each site. Zooplankton sampling from Burullus Lake was obtained by filtering 50 L of water through a small standard net (mesh size 55 µm) using a 10 L container. The collected samples were preserved directly with 4% neutral formalin solution in 250 mL polyethylene bottles. The volume of all samples was concentrated to 100 mL, and the whole sample was examined in a Petri dish under a research binocular . For zooplankton count purposes, at any rate, two aliquots (2 mL of well-shaken suspension) were removed from each example utilizing a graduated pipette, set in an including chamber, and the number of individuals of every species was enumerated. The average number of duplicated assessments for each example was assessed, and enumerations were communicated as the number of organisms per cubic meter [11]. The organisms were identified and counted. The total number of zooplankton present in a cubic meter (m3) of water sample was calculated according to the following equation: [24] N= n (v/V) ∗ 1000 (1) where N = total number of zooplankton per cubic meter of filtered water; n = average number of zooplankton in 1 mL of zooplankton sample, v = volume of zooplankton concentrates (ml), V = volume of total water filtered (L). DiversityDiversity 20212021,, 1313,, x 268 FOR PEER REVIEW 44 of of 23 23

FigureFigure 1. 1. LocationLocation map map of of the the study study area. area.

TableTable 1. SitesSites description description in in Burullus Burullus Lake. Coordinates Site No. Description Coordinates Site No. Description N E NE 1 In front of East El-Burullus drain 31.0826 31.5529 1 In front of East El-Burullus drain 31.0826 31.5529 2 In front of El-Boughaz 30.9789 31.5771 3 2 In front ofEl-Bellaq El-Boughaz 30.978930.9986 31.577131.5456 4 3 In front El-Bellaq of drain 7 30.9986 30.9610 31.5456 31.4520 5 4 In frontEl-Zanqa of drain 7 30.961030.8047 31.452031.4982 6 5 El-ZanqaEl-Maqsaba 30.804730.7519 31.498231.4784 7 6 El-MaqsabaEl Shakhlouba 30.751930.7575 31.478431.4028 8 7 El ShakhloubaMastrou 30.757530.7134 31.402831.4583 9 Abou Amer 30.6806 31.4281 8 Mastrou 30.7134 31.4583 10 El-Berka El-Gharbia 30.6325 31.4160 9 Abou Amer 30.6806 31.4281 11 In front of drain El-Hoks 30.6065 31.3831 1210 In El-Berka front of El-Gharbia Brinbal Canal 30.6325 30.5854 31.4160 31.4009 11 In front of drain El-Hoks 30.6065 31.3831 2.2.3. Trophic12 State Index In(TSI) front of Brinbal Canal 30.5854 31.4009 Carlson’s (TSI) is used to provide a single assessable index for classifying lakes according to the trophic state of the lake. Recently, Carlson's index has 2.2.3. Trophic State Index (TSI) been usually accepted in the limnological community as a reasonable approach for this problem.Carlson’s It is used trophic as an state assessment index (TSI) of the is trophic used to state provide for a amarine single body assessable by some index water for qualityclassifying factors lakes containi accordingng: to the trophic or transparency state of the by lake. the Recently,concentrations Carlson’s of Secchi index disk has depthbeen usually(SD), ortho-phosphate accepted in the (PO limnological4), and chlorophyll-a community (Chlo-a as a reasonable) [25]. The higher approach values for cor- this respondproblem. to It the is used increase as an in assessment fertility, which of the shows trophic further state foreutrophic a marine conditions. body by some Each water aug- mentsquality in factors TSI via containing: 10 units relates turbidity to a decrease or transparency in the Secchi by the disk concentrations (SD) transparency of Secchi through disk moietydepth (SD),and augment ortho-phosphate in the concentration (PO4), and of chlorophyll-a phosphorus via (Chlo-a double.)[25 The]. The spatial higher proration values ofcorrespond the TSI data to was the increaserecorded in by fertility, the ordina whichry Kriging shows methodology further eutrophic [25] as conditions. follows: Each augments in TSI via 10 units relates to a decrease in the Secchi disk (SD) transparency

Diversity 2021, 13, 268 5 of 23

through moiety and augment in the concentration of phosphorus via double. The spatial proration of the TSI data was recorded by the ordinary Kriging methodology [25] as follows:

CTSI = [TSI (TP) + TSI (CA)]/2 (2) The formulas for calculating TSI values from TP and Chlo-a are:

a- TSI for Chlorophyll-a (CA) TSI = 6 − [(2.04 − 0.68 (chl − a))/(Ln (2)] (3)

b- TSI for Total phosphorus (TP) TSI = 10[6 − (21.67/po4)/(Ln (2)] (4) −1 where Ln is natural logarithm. Po4 is dissolved phosphorus in (µg L ), Chlo-a is chlorophyll- a, in (µg L−1). The TSI index was calculated using Carlson’s trophic status index as the most important, in addition to the popular TSI process designated for the present research [26]. On the Carlson’s scale, if TSI is <30 characterizes oligotrophic, from 30 to 50 characterizes mesotrophic, from 50 to 70 eutrophic, and >80 hypereutrophic. Ecological risks of nitrogen and phosphorus were evaluated by using the following equation of the trophic index (TRIX) [1]:

TRIX = (LOG (Chlo-a × [% DO] × DIN × SRP + 1.5))/1.2 (5)

where SRP, DIN, and Chlo-a are the concentrations of soluble reactive phosphorus, dis- solved inorganic nitrogen, and chlorophyll-a, respectively. A percentage of DO is the absolute results of deviation and is calculated as [100% DO]. Trophic index levels were defined in following Table2.

Table 2. Trophic index levels.

Level Value Water Quality State Low TRIX < 4 excellent Moderate trophic level 4 < TRIX level < 5 very good High trophic level 5 < TRIX < 6 good Very high trophic level TRIX > 6 fair

2.2.4. Water Quality Index (WQI) The water quality index (WQI) is described as a technique of rating that provides the composite effect of individual water quality factors on the general water quality [23]. The pollution index is a beneficial approach to give information about water quality. It was described as a rating reflecting the compound effect of different water quality factors on the total quality of water [27]. WQI is a mathematical way of summarizing multiple properties into a single value. Moreover, WQI is useful for comparing alterations in water quality across a region, or for measurement changes in water quality over time. In the current study, WQI was calculated using the equation developed by Tiwari and Manzoor [28]. The quality rating (qi) for the water quality factor was obtained by the following relation [28]:

qi = 100 × [Vi/Si] (6)

where Si is the standard of the stream water quality, and Vi is the observed data of the factor at a known sampling site according to all parameters. The equation confirms that qi = 100 if the presented data are impartial and equal to its standard data. Therefore, the larger data of qi revealed polluted water. To compute the WQI, the quality rating qi corresponding to factor can be delimiting using Equation (6):

WQI = Σ qi (7)

where i = 1. The average water quality index (AWQI) for n factors was computed using the following equation: AWQI = Σqi/n (8) Diversity 2021, 13, 268 6 of 23

where n = number of factors. AWQI was classified into 4 categories: good (0.0–100), medium (100–150), bad (150–200), and very bad (over 200).

2.3. Descriptive Statistics The relationships between different factors were calculated from the correlation ma- trix formed in IBM SPSS statistics, version 22 programs. The correlation coefficients are considered significant at 0.01 levels (2-tailed) and 95% confidence level (p ≤ 0.05). Statisti- cal for zooplankton was performed by the primer 5 (Plymouth Routines in Multivariate Environmental Research) program to measure both the Shannon index (H), the evenness index (E), (D), and the similarity index.

3. Results and Discussion 3.1. Water Characteristics and Physicochemical Parameters The physicochemical parameters recorded at the sampled stations from 2017 to 2019 are summarized in Table3. The temperature value is a crucial parameter for all biological processes [16]. The mean water temperature in the lakes fluctuated between a minimum mean value of 14.47 ◦C in the winter season of 2018 and a high of 31.23 ◦C in the summer. In the current study, the maximum value was observed in the year 2017 in the summer season, and the annual average of three years was 21.77 ◦C. According to EPA [29], the water temperature ranged from 15.1 to 32.6 ◦C in lake water, which is suitable for fish growth.

Table 3. The annual averages, minimum, and maximum values of physicochemical parameters.

Year Max Min Average Parameter * 2019 2018 2017 31.23 14.47 21.77 19.11 24.21 22.01 Temp ◦C 9.36 7.32 8.09 8.18 7.56 8.55 pH 38.91 0.62 4.60 3.94 3.88 6.00 Salinity‰ 19.87 0.9 8.83 10.23 8.58 7.68 DO (mg L−l) 176.66 1.67 23.63 24.09 22.53 24.29 BOD (mg L−l) 423.98 30.12 100.39 151.31 59.98 89.88 COD (mg L−l) −l 4.45 0.013 0.61 0.66 0.47 0.71 NH4 (mg L ) −1 419.71 2.98 126.95 116.21 131.55 133.1 NO2 (mg L ) −l 1.64 0.013 0.283 0.35 0.19 0.31 NO3 (mg L ) 10.33 0.52 3.40 5.04 2.15 3.03 Total N (mg L−l) 2105.77 60.96 640.56 1017.88 399.8 504.01 Total P (µg L−l) 383.81 6.25 62.93 70.69 70.71 47.39 Chlo-a (µg L−l) * Temp: temperature, DO: dissolved oxygen, BOD: biological oxygen demand, COD: chemical oxygen demand, NH4: ammonia, NO2: nitrite, NO3: nitrate, TN: total nitrogen, Total P: total phosphorus, Chlo-a: chlorophyll-a.

The pH values can affect the biological activities of microbial metabolites that can influence the further utilization of succeeding metabolic products. In the current study, the values of pH of water samples ranged between 7.32 and 9.36 with an annual mean of 8.09. The highest value was observed in front of El-Kashaa drain in the summer season of 2017, while the lowest result was noted at station 11 in the winter season of 2019. According to the annual average values, the hot season (summer) recorded a higher pH level than the cold season (winter), which is correlated, mainly, to the increase in CO2 uptake because of the rise in the photosynthetic activity, which leads to high pH values [3,30]. High pH values occur according to the of effluent in the lake in addition to the fermentation process, decay of organic matter, and release of organic acids Diversity 2021, 13, 268 7 of 23

by bacterial activity [28]. These results were in the same ranges stated by Okbah and Hussein [31]. El-Alfy et al. [32] at the Burullus Lake showed that the dominant alkaline pH was >7.0. Additionally, Khairy et al. [33] showed that the average of pH values in Burullus Lake was 8.1. Salinity has a significant influence on measuring numerous conditions of the aquatic biological processes and the chemistry of natural waters [34,35]. In the present study, salinities exhibited wide variations between 0.62 and 38.9‰, with the maximum value being noted in station 2, in front of El-Boughaz in 2017 in the winter season; whereas, the highest values were related to marine water intrusion along the Boughaz area. Conversely, the lowest value was recorded in front of drain El-Hoks (station 11) in 2018 in the summer season, with an average value of 0.62‰. Low salinity values indicate that the water content in the lake was mainly freshwater due to human activities and the quantity and quality of drainages runoff in the lake. Salinity distribution in the lagoon water reflects a decreased gradient from the east to the west. This gradient depends on the amount of drainage water that comes from the south drains, fresh Nile water from Brimbal Canal at the west, and sea water from the sea outlet at the east, and therefore, marine plankton species are restricted only in the eastern basin and in some cases dominate the community. According to previous references, the salinity of the lagoon increased from year to year, which creates high conditions especially in the eastern basin (>17 PSU) [36]. El-Shinnawy [37] reported that the high salinity and presence of marine forms in the eastern basin at Burullus Lake could be due to the closure policy of the pumping drain stations, which diminish the water level to be below sea level and permits seawater to enter the lagoon. As well, Nassar and Gharib [38] reported that the average salinity of the Burullus Lake in the year 2013 was 3.6‰. Dissolved oxygen (DO) is considered as one of the maximum important factors controlling the biota in the aquatic [16]. In the current study, DO values varied from 0.9 to 19.87 mg L−1. The higher value was obtained at the front of El-Kashaa drain in the year 2017 in the summer season, while the lowest value was documented at station 11 in the winter season of 2018, with an annual mean of the study period of 8.83 mg L−1. Under low dissolved oxygen, many marine and may not survive [39]. The decrease in oxygen supply in the water showed a negative effect on aquatic life. The highest value occurs during the summer season due to the increase in photosynthetic activity during this season, which liberates an important quantity of oxygen to the surrounding water ecosystem, since the photosynthetic method was regarded as the highest source of oxygen in the aquatic environment [33]. Moreover, the quantity of DO in water could be based on the salinity and temperature of the water, as cold liquid can hold more DO than warmish liquid [40]. These results agreed with those achieved by Hereher et al. [41] and Khairy et al. [33] who showed that the average concentration of DO along the Burullus Lake was 7.6 mg L−1. Biological oxygen demand (BOD) gives data on the biological convertible amount of the content of organic content in marine samples. In the current work, BOD in the lakeshores habitat varied from 1.67 to 176.60 mg L−1, with an average value of 23.63 mg L−1. The maximum value was recorded at station 9 (Abou Amer) in the year 2018 in the autumn season, and the lowest result was showed in facing the El-Boughaz outlet in the spring season of 2019 due to the dilution effect of low organic matter loaded seawater. BOD values of 3 mg L−1 indicate pure water, but values that reach 5 mg L−1 give an indication of doubtful purity of water [42]. The high values of DO may be because of the abundance of plankton, which enhanced water quality with oxygen throughout photosynthesis ac- tivity [15,43,44]. In addition, augmented oxygen reduction is essential for oxidation of the organic matter in the aquatic body [45,46]. Younis and Nafea [47] recorded that the concentration of biological oxygen demand in the water samples at Burullus Lake ranged from 11.7 to 36.66 mg L−1. Chemical oxygen demand (COD) is an important parameter for determining the quality of water and wastewater quality. The COD is used to monitor Diversity 2021, 13, 268 8 of 23

efficiency. In the current study, COD showed different values between different habitats. It varied from 30.12 to 423.98 mg L−1. The maximum value was recorded in the year 2018 in the winter season, and the lowest value was recorded in the year 2018 in the autumn season, with an annual average value of 100.39 mg L−1. The permissible limit for COD in marine water is 100 mg L−1 [48]. The average data of COD parameter in all environments were exceeding 40 mg L−1, hence the lake is measured as polluted water as reported by Hassan et al. [45] who stated that water bodies contain COD > 40 mg L−1 are considered as polluted waters; however, those containing COD > 120 mg L−1 are extremely polluted. Nitrogen and phosphorous are the nutrients most likely to remain deficient in the contaminated environment. Nutrients from anthropogenic pollution can degrade water quality and alter the balance of marine food webs [16,19]. Ammonia (NH4) contents in the water of lakeshores habitat varied from 0.013 to 4.45 mg L−1, which was the maximum value recorded in station 7 in front of downstream 8 and 9 drains in the winter season in the year 2017. The annual average value during the three-year period of the study was 0.613 mg L−1. The minimum values may be related to increases in plankton . The high population in water bodies utilizes a high content of ammonium ions in preference to other inorganic nitrogen [49]. Our results agree with Okbah and Hussien [25], who showed that in the regional variations of NH4, the minimum mean −1 concentration was 3.70 µmol L . In contrast, the maximum mean value of NH4 was 12.33 µmol L−1. Nitrite (NO2) is the noxious via-creation of nitrifying (nitrospiration) in substrate consuming NH3 or a filter. In the current study, nitrite ranged from 2.98 (summer season) to 419.71 mg L−1 in station 6, in the spring season in the year 2018, with a mean value throughout the three-year stage of this study of 126.93 mg L−1. The highest value of water nitrite is related to human activities of diverse origin mainly from domestic drainage. It also occurs due to the nitrification of free ammonia and a reduction in nitrate to nitrite and use of ammonium . Minimum values of nitrite are explicating to these places that are far away from any pollution sources. Nassar and Gharib [38] recorded that the −1 average concentration of NO2 in Burullus Lake was 0.1 µmol L . Nitrate (NO3) is considered as the most stable and predominant inorganic nitrogen form in seawater, in addition to major nutrients for the phytoplankton growth [50]. Nitrate serves as another electron acceptor under anoxic conditions. The present values of nitrate ranged from 0.13 to 1.64 mg L−1. The present study found that the highest value of nitrate was observed in the year 2017 in the winter season in station 6 in the north of the lake. The increase in nitrate values may be attributed to the discharge of wastes and the increase in mineralization of organic matter. Additionally, it is noticed that the high results of nitrate are related to drainage 9 and 8 of the agricultural wastewater that are loaded by high amounts of nitrogenous fertilizers, discharged into these sites. The minimum value was recorded in station 5 in the middle of the lake, which related to the increase in aquatic plants that feed on nutrients and cause depletion in their concentration [51–53]. Abd El-Hamid [54] reported that NO3 concentrations in water samples at Burullus Lake ranged from 0.15 to 0.47 mg L−1. Total nitrogen (TN) concentration in the investigated area showed narrow variation, ranging between a minimum value of 0.52 mg L−1 at sampling site 2 in front of El-Boughaz in the summer season and a maximum value of 10.33 mg L−1 at El-Shakhlouba in the winter season as a result of the effect of industrial, agricultural, and demotic wastes through drains 8 and 9, with an average concentration of 3.40 mg L−1. It is obvious that the water of this lake surrounds a considerable quantity of particulate nitrogen related to organisms and products of their , besides decay [31]. These results agree with El-Zeiny and El-Kafrawy [55]; they showed that the highest concentrations of TN have been noticed in the parts polluted by , run-off animal wastes, and domestic sewage at the southeastern and western part of the lake. Diversity 2021, 13, 268 9 of 23

Phosphorous is needed for the formation of cellular enzymatic compounds used in the processes of synthesis and degradation. The most common sources of phosphorous in bacterial sources are K2HPO4, KH2PO4, NaH2PO4, Na2HPO4, or mixtures of them [56]. The current results found that total phosphorus content showed its high values in water in the year 2019, with a high value (60.96 mg L−1) in winter in station 7 and a low value (2105.77 mg L−1) in summer in station 2 at summer season. While the annual average through the three-year time of the study was 607.23 mg L−1. Maximum values are related to industrial effluents and domestic sewage disposal to these sites. In contrast, the minimum values are related to an increase in plankton, which feed on nutrients and cause depletion in its concentration [56]. El-Zeiny and El-Kafrawy [55] documented that the concentration of total phosphorous in Burullus Lake ranged from 4.42 to 53.6 mg L−1. Chlorophyll-a (Chlo-a) is considered as the main pigment that can be used for the determination of phytoplankton biomass, and it is used as a trophic state indicator and reflected the water quality in the ecosystem [57]. In the current study, the Chlo-a contents ranged from 6.25 to 383.81 µg L−1. The average value for three years was 62.93 µg L−1. In general, the higher result was found in station 4 in front of drain 7 in the autumn season, while the lowest value was exhibited at station 2 in the spring season of 2017. The high values of Chlo-a in the investigated area are undoubtedly due to the rich supply of reactive and reactive phosphate; these nutrient salts contribute to the growth of phytoplankton expressed in high levels of Chlo-a, which lead to the eutrophication process in the Lake. Abd El-Hamid et al. [54] reported that chlorophyll-a concentrations in aquatic samples of Burullus Lake ranged from 3.1 to 108 µg L−1. Generally, it is notable that regarding the Chlo-a and NH4 in Burullus Lake, the minimum results were recorded at the northern part of the lake especially in the next El- Boughaz part due to it receiving water from the sea by the Al-Boughaz outlet. On the other hand, the maximum values of Chlo-a and NH4 were noted at the southern part of Burullus Lake; this may be due to a dense population of phytoplankton as a result of the huge amounts of discharged wastewater that is heavily loaded with nutrient. Moreover, NH4, TN, and total P exhibited high contents in station 7 in front of drains 8 and 9 compared with the sampling sites.

3.2. Heavy Metals The maximum, minimum, and average concentrations of heavy metal ions in the water samples collected from Burullus Lake are shown in Table4.

Table 4. The annual averages, minimum, and maximum values of metals concentrations.

Year Averages Max. Min. Annual Average Metal * 2019 2018 2017 220.71 6.68 49.29 18.25 72.65 56.99 Fe (µg L−1) 34.65 1.64 8.81 3.16 17.77 5.5 Cu (µg L−1) 34.56 0.12 11.28 11.06 6.12 16.66 Zn (µg L−1) 34.98 2.29 10.19 11.35 16.01 3.21 Cr (µg L−1) 12.98 1.59 5.44 4.31 6.79 5.23 Ni (µg L−1) 3.35 0.04 1.18 0.43 1.82 1.31 Cd (µg L−1) 18.51 0.29 4.87 0.98 6.31 7.32 Pb (µg L−1) * Fe: , Cu: copper, Zn: zinc, Cr: chromium, Ni: nickel, Cd: cadmium, and Pb: lead ions.

The different heavy metals, including Pb3+, Cr3+, Ni2+, and Cd2+, are toxic ions to living organisms even at quite low concentrations, whereas Zn2+ and Cu2+ are more biolog- ically essential as natural constituents of aquatic ecosystems and, generally, only become toxic at very high concentrations. Heavy metals are normally entering the aquatic environ- ment through of the geological matrix, or due to anthropogenic activities caused Diversity 2021, 13, 268 10 of 23

by industrial effluents, domestic sewage, and wastes [58]. Fe2+ compounds in aquatic environments resulting in Fe2+ precipitate in alkaline and oxidizing conditions [34]. In the current work, the Fe2+ values in the water varied from 6.68 to 220.71 µg L−1. The maximum value was recorded in the year 2018, while the annual average for three years was 49.29 µg L−1. The high concentration of oxygen leads to Fe2+ oxidation and subse- 2+ quent hydrolysis to form insoluble Fe(OH)3. The maximum concentration of Fe observed in the current study may be due to the industrial wastewater discharged to the coastal area of the Mediterranean Sea. High levels of Fe2+ may decrease the microbial degrada- tion of hydrocarbon in seawater because excessive concentrations break down enzyme action [59]. Eid et al. [60] found that Fe2+ concentrations in Burullus Lake were high during the growing season. Copper complexation in water is affected by dense phytoplankton blooms [61]. In the current study, the mean values of Cu2+ content in Burullus Lake ranged from 1.64 to 34.56 µg L−1. The maximum value was recorded in the year 2017 in station 7, and the annual average of the three years was 8.81 µg L−1. The maximum concentration of Cu2+ may lead to a negative impact on microbial degradation of hydrocarbon in seawater, which excessively breaks down the action of the enzyme [62]. Nafea and Zyada [63] noticed that the concentration of copper content in the water of Burullus Lake ranged between 19.2 and 35.8 36.9 mg L−1. Zinc is an essential ion for the growth of marine organisms, and its concentration is affected by plankton communities [59]. The current work observed that Zn2+ showed its high mean value in water (34.56 µg L−1) in station 2 in the year 2017 and the low one (0.12 µg L−1), and the average low value was 11.28 µg L−1. The relatively high Zn2+ level is suggestive of the influence of refuse dump and domestic sewage sources. It could also be attributed to industrial effluents and . High temperature and low dissolved oxygen concentration lead to an increase in of Zn2+ [22]. Cr is one of the biochemically active transition metals in the aquatic environment [64]. In the current study, dissolved chromium values in the water of the lake varied from 2.29 to 34.98 µg L−1. The maximum value was recorded in 2019, and the annual average of three years was 10.19 µg L−1. The values in the lake are within the EPA limit (100 µg L−1)[64]. Cr oxidizes easily from trivalent to hexavalent. Cr3+ ion is not toxic, but an essential nutrient, but Cr6+ ion is very toxic and may damage adrenals, livers, and lungs. Ni2+ contents in water bodies are attributed as results from industrial and urban activities and may accumulate in many types of fishes and macrophytes [65]. In the current study, Ni2+ ions contents ranged between 1.59 and 12.98 µg L−1. The maximum value was observed in the year 2018, and the annual average of three years was 5.44 µg L−1. The higher value of Ni is associated with Fe and Mn, because of the fact that Ni2+ has been scavenged directly from water by hydrous MnO2 [59]. El-Amier et al. [64] showed that nickel concentration along Burullus Lake ranged from 1.26 to 9.37 µg L−1 with an average value of 5.10 µg L−1. Cd2+ is one of the greatest poisonous metals with widespread carcinogenic effects in humans and is considered to be toxic if its concentration exceeds 0.01 mg L−1 both in drinking and irrigation water [9,12]. Cd2+ ions are extremely toxic to fish. Cd2+ contents ranged from 0.04 to 3.35 µg L−1 in front of Burullus east drain in the year 2018 as a result of agricultural wastes, especially agricultural fertilizers, and the annual average was 1.186 µg L−1. Pb2+ is a very significant ion in the aquatic system [66]. Lead contents in the current study showed its high mean values in water (18.51 µg L−1) at station 7 in the year 2019, while it showed a low mean value of 0.29 µg L−1 with annual averages from three years of 4.87 µg L−1. The highest values of lead can disrupt the health system of phytoplankton, which is an important source of oxygen production in seas. The great level of lead may be attributed to the agricultural and industrial effluents in addition to the spill of fishing boats, which are distributed along the coast of the study area. However, many have been painted by a dye containing a high concentration of Pb2+ metal. Pb2+ in high concentrations causes hemorrhages and congestion of the gastrointestinal tract and kidneys of fish [67]. Diversity 2021, 13, 268 11 of 23

Masoud et al. [68] recorded that the concentration of lead content along Burullus Lake ranged from 4.5 to 10.1 µg L−1.

3.3. Water Quality Indices and Carlson Trophic State Index The water quality index (WQI) is the most effective way to communicate water quality. The present values of WQI and AWQI were calculated according to standard limits of drinking water parameters of WHO [22] (maximum permissible limits), as presented in Table5. Average WQI values along Northern Delta Lake Burullus across three years were 80.67, 68.23, and 90.24, for the years 2017, 2018, and 2019, respectively. In general, this means that the waters of Burullus Lake are classified under good water quality (suitable for all uses) during the sampling period at most sites. Contamination levels of the water of Burullus Lake are coved by industrial effluents, untreated domestic and sewage water coming from drainage water. Eutrophication and organic pollutants are still the major pollution problems in aquatic environments. Eutrophication is the method by which aquatic lakes are supplemented with nutrients, increasing the production of rooted aquatic plants and to levels considered to be an interference with desirable water uses such as recreation, fish maintenance, and water supply [26].

Table 5. Water quality indices and average water quality indices of Burullus Lake water.

2019 2018 2017 Si Parameter qi Vi qi Vi qi Vi 96.23 8.18 88.94 7.56 100.58 8.55 8.5 pH −1 330 0.66 235 0.47 355 0.71 0.2 NH3 (mg L ) 204.6 10.23 171.6 8.58 153.6 7.68 5 DO (mg L−1) −1 0.77 0.35 0.42 0.19 0.68 0.31 45 NO3 (mg L ) 151.31 151.31 59.98 59.98 89.88 89.88 100 COD (mg L−1) 6.08 0.018 24.21 0.0726 18.99 0.056 0.3 Fe (mg L−1) 0.22 0.011 0.12 0.0061 0.333 0.01666 5 Zn (mg L−1) 0.316 0.003 1.77 0.017 0.55 0.0055 1 Cu (mg L−1) 22.7 0.01 32.02 0.016 6.42 0.00321 0.05 Cr (mg L−1) 812.24 614.07 726.05 WQI 90.24 68.23 80.67 AWQI

According to average TSI values during the period from 2017 to spring 2019, the Burul- lus Lake in this study is classified as hypertrophic, as shown in Table6. This classification is a result of different human activities, domestic, industrial sewage, and agricultural runoff from the River Nile and their related drainage systems. This causes over-enrichment of nutrients in the water bodies leading to algal blooms. The decaying method of dead alga can produce the exhaustion of dissolved oxygen in the aquatic lake producing an anoxic environment [14].

Table 6. Carlson’s trophic state index of Burullus Lake during the sampling period.

Year [TSI] PO4 [TSI] C [TSI] SD Average [TSI] Tropic State 2017 93.87 155.91 326.06 191.95 Hypereutrophic 2018 90.53 172.08 325.13 195.91 Hypereutrophic 2019 104.01 172.07 324.18 200.09 Hypereutrophic

The water quality index provides a convenient means of summarizing complex water quality data. To recognize the trophic condition of Lake Burullus, the trophic index (TRIX) Diversity 2021, 13, 268 12 of 23

of water quality was calculated [69]. It is a linear mixture of four state factors correlated to the primary production of oxygen and chlorophyll-a, in addition to nutritional conditions, for example, inorganic phosphors and dissolved inorganic nitrogen [70]. This scale was associated with the four-category scales for water quality state: excellent, very good, good, and fair [17]. According to the seasonal assessment of TRIX and Carlson’s trophic state indices, the sites are categorized at a high eutrophic level in most stations for three years, as shown in Table7, revealing the existence of anthropogenic pressure. Very high trophic level exposed high nutrient levels, low transparency, and recurrent /anoxia in bottom waters [1].

Table 7. TRIX and Carlson’s trophic state indices.

Year TRIX Indices Values Trophic State 2017 5.94 high trophic level 2018 5.22 high trophic level 2019 5.43 high trophic level

3.4. Zooplankton Community Zooplankton serve in the evaluation and of the ecosystem, since they are considered as an essential food for other organisms. The studies of the distributions of zooplankton are beneficial for the monitoring of definite characteristics of the environment such as hydrographic, pollution, eutrophication, and long-term changes, which are signs of environmental disturbances. Therefore, zooplankton studies becoming very important in both marine and freshwater ecosystems [27,28]. In the current study, the comparison among the three years (2017 to 2019 seasons) in the distribution, density, and occurrence of zooplankton was conducted. The zooplankton assemblage was dominated by Rotifera, Copepoda, Protozoa, and Cladocera, respectively, while other groups have rare occurrence so appear and disappear in different years and stations. Over the study period, mean zooplankton density was higher in the western basin (333,579 ind. M−3) in the same trend with Khalil [71], Dumont and El-Shabrawy [72] and Saad et al. [73]. The middle and eastern basins (290,707 and 142,978 ind. M−3, respectively) may be increased for phytoplankton in this area [28], while mean zooplankton density was higher in the 2017 year (301,664 ind. M−3) than the 2019 and 2018 years (238,703 and 226,897 ind. M−3, respectively) as shown in Table8.

Table 8. Mean zooplankton in three years at Burullus Lake.

Basin Year Protozoa Rotifera Copepoda Cladocera Others Mean Eastern 2017 5417 919,000 143,750 6000 41,833 223,200 2018 21,500 400,583 120,000 16,000 18,167 115,250 2019 15,833 180,000 79,917 174,000 2667 90,483 Middle 2017 8750 1,556,100 280,000 83,500 7050 387,080 2018 6900 1,264,000 137,850 65,550 3900 295,640 2019 38,850 743,650 107,800 48,900 7800 189,400 Western 2017 8250 1,097,688 350,813 11,250 5563 294,713 2018 5375 1,213,000 128,250 1000 1375 269,800 2019 28,875 1,915,250 207,250 4875 24,875 436,225 Mean 2017 7472 1,190,929 258,188 33,583 18,149 301,664 2018 11,258 959,194 128,700 27,517 7814 226,897 2019 27,853 946,300 131,656 75,925 11,781 238,703

In 2017, a total of 93 taxa from 52 genera and 10 groups were noted for the study, namely, Protozoa (16 taxa); Rotifera (34 taxa), the same number in Saad et al. [73], the domi- nant species being angularis, Brachionus calyciflorus, and Keratella valga; Copepoda Diversity 2021, 13, 268 13 of 23

(28 taxa), the dominant species being Acanthocyclpos vernalis, Mesocyclops leuckarti, and Thermocyclops crassus; Cladocera (nine taxa), the dominant species being hyaline and Daphnia longispina, and taxon for each of Ostacoda, Cirripeda, Nematoda, , Decapoda, and Velliger of lamellibranchs. In 2018, a total of 98 taxa from 59 genera and 10 groups with larvae were documented for the study, namely, Protozoa (20 taxa from 16 genera); Rotifera (35 taxa), the domi- nant species being Brachionus angularis, Brachionus calyciflorus, Keratella valga, and Keratella quadrata; Copepoda (28 taxa), the dominant species being Acanthocyclpos vernalis, Mesocy- clops leuckarti, and Thermocyclops crassus; Cladocera (nine taxa), the dominant species being Moina micrura, and taxon for each of Ostacoda, Cirripeda, Nematoda, Annelid, Decapoda, and Velliger of lamellibranchs. In 2019, a total of 98 taxa from 59 genera and 10 groups with larvae were detailed for the study, namely, Protozoa (20 taxa from 16 genera); Rotifera (35 taxa), the domi- nant species being Brachionus angularis, Brachionus calyciflorus, Keratella valga, and Keratella quadrata; Copepoda (28 taxa), the dominant species being Acanthocyclpos vernalis, Mesocy- clops leuckarti, and Thermocyclops crassus; Cladocera (nine taxa), the dominant species being Moina micrura, and taxon for each of Ostacoda, Cirripeda, Nematoda, Annelid, Decapoda, and Velliger of lamellibranchs. While, Shaltout [74] recorded 90 taxa in Burullus Lake. The lowest population densities of zooplankton at the sites of the eastern sector are perhaps due to their vertical migration far of sunlight. Many authors concluded that the zooplankton has a high population density in the summer season, but their lowest one happens in winter [14,16,75]. Additionally, it is difficult to distinguish between the effects of most environmental factors on the abundance at most aquatic ecosystems due to inter-relation between them; also, the biological and ecological factors have the same effects of environmental factors on zooplankton abundance inside any aquatic system [12,76]. So, it is not surprising that the standing crop of zooplankton decline in autumn, although environmental conditions are good; this is perhaps due to the great amounts of fish fries that are received at these zones. Heneash et al. [77] reported that Copepoda were related (twice) mainly to domestic activities, while Rotifera were related to activities [12,16].

3.5. Biostatistics for Seasonal Zooplankton Population The data representing the diversity indices of the stations calculated from annual data are presented in Table9. The total of species, in general, ranged between 16 in the middle sector in 2018 to 29 species in the western sector in 2019. The index of richness was found to be varied between 0.1 in the eastern sector St. 1 in 2018 and 2.14 in the western sector St. 9 in 2019. The results of the Evenness index analysis showed that the value was 1.0 to all stations except for stations number 1 and 3 in the eastern sector in 2018. The values of the Shannon index varied between 0.67 in the western sector St. 12 in 2018 and 2.50 in the middle sector St. 5 in 2019. Saad et al. [78] reported that the population density of zooplankton was noticeably higher in the western part of the lake, with a major peak of an average of 1,764,333 org. m3. Moreover, regarding seasonal variation, there was a gradual growth in zooplankton standing crop from a minimum of 523,300 org. m3 in autumn until reaching a maximum of 1,353,182 org.m3 in summer, with an overall average of 902,911 org. m3.

3.6. Similarity between Sites During the year 2017, the data indicated the presence of three clusters (Figure2A). The first cluster included station 3 in the seaside of El-Burullus Boughaz with relatively low similarity to the other stations being 75% on average. The second cluster included three stations 9,4, and 10 with 92% similarity between them, but a sub-cluster was found between stations 4 and 10 with 97.5% being the highest similarity in this period. However, the third cluster included other stations being 86% (stations 7, 8, 1, 5, 12, 2, 6, and 11). However, this cluster contains three sub-clusters (between stations 7and 8, sub-cluster station 1, sub-cluster between 5, 12, 2, 6, and 11). Diversity 2021, 13, 268 14 of 23

During the year 2018, the data indicated the presence of four clusters (Figure2B). The first cluster included station 3 in the seaside of El-Boughaz with relatively low similarity to the other stations being 76% on average. The second cluster included station 1 with 82% on average near to El-Boughaz. The third cluster included six stations with 88% (stations 12, 9, 10, 11, 2, and 4), and the highest similarity was between station 9 and 10 with 98%. The fourth cluster was between stations 7, 8, 5, and 6, but the highest similar one was between 5 and 6 with 94%. During the year 2019, the data were found to be similar to that obtained in 2018 with slight differences in the arrangement of stations. Four major clusters were documented during this year. The first cluster was El-Boughaz station 3 with 76%. The second cluster included three stations with 81% on average nearby El-Boughaz. The third cluster included some the rest of the stations with four sub-clusters. The first included station 12, which had 93.5%. The second sub-cluster was between stations 9 and 10, with 98% highest similarity. The third sub-cluster included stations 11 with 90% (Figure2C). The fourth sub-cluster was between stations 2 and 4 with 93% on average. The fourth cluster was between stations 7, 8, 5, and 6, but the highest similarity was between 5 and 6 with 94%. The changes in the character of the water are also reflected in the zooplankton pop- ulation. Changes in the zooplankton population may be due to the changes in water conditions, introducing freshwater species and eliminating marine ones. Dumont and El-Shabrawy [72] conclude that, from the early onset of dam construction in the Nile valley, slight changes happened in the zooplankton of Lake Burullus and three other delta lakes.

3.7. Spatial and Temporal Patterns of Zooplankton Community Zooplankton density was higher in the western basin with value 333,579 ind. m−3 than in the middle and eastern basins (290,707 and 142,978 ind. m−3, respectively); this may be due to the increase in phytoplankton in this area, and it is near freshwater sources as reported by Saad et al. [78]. However, mean zooplankton density was higher in the 2017 year (301,664 ind. m−3) than in 2019 and 2018 (238,703 and 226,897 ind. m−3, respectively). Seasonally, at both eastern and middle sectors, the autumn season recorded the highest mean in 2017 and 2018, but in the 2019 summer season, we found a high abundance of zooplankton. In the western sector, in winter, we registered the highest zooplankton abundance (Figure3 and Table 10).

3.8. The Correlation between Physicochemical Parameters and Zooplankton Groups Correlation analysis was achieved by Pearson’s correlation coefficient. The correla- tion matrix was calculated for the water quality parameters. A result of the correlation coefficient was evaluated as follows: 0.0 (no); 0.3–0.5 (low); 0.5–0.7 (medium); 0.7–0.9 (high); 0.9–1 (very high). In the present study, there were high significant correlations between many parameters such as Protozoa with Rotifera, Cirriped larvae, Velliger of lamellibranchs, salinity, and Zn ions (r = 0.925, 0.991, 0.946, 0.998, 0.897, respectively). Rotifera also showed a significant correlation with Copepoda, Cirriped larvae, pH, salinity, Chlo-a, and Pb ions (r = 0.954, 0.984, 0.925, 0.968, 0.961, 0.814, respectively). There is a significant positive correlation between Copepoda and Cirriped larvae, Velliger of lamelli- branchs, salinity, and Zn ions (r = 0.992, 0.944, 0.999, 0.894, respectively). Cirriped larvae correlated negatively and some parameters such as salinity, NO3, and Chlor-a (r = −0.995, −0.970, −0.999, respectively). Ostracoda showed a negatively significant correlation with BOD, NH4, NO3, and Fe (r = −0.995, −0.981, −0.970, −0.959, respectively). Cladocera correlated positively with parameters such as Ostracoda and Annelida with r = 0.97 and 0.94, respectively; while, it correlated negatively with parameters such as BOD, NH4, NO3, and Fe ions (r = −0.041, −0.91, −1.00, −0.999, respectively). Diversity 2021, 13, 268 15 of 23

Table 9. Biostatics for seasonal zooplankton in 2017–2019.

Basin/Station Species No. Indi. m−3 Richness (d) Evenness (j) Diversity (H) 2017 St. 1 15 1,592,750 1.02 0.54 1.48 Eastern St. 2 19 1,171,000 1.31 0.68 1.91 St. 3 15 584,250 1.05 0.66 1.65 St. 4 19 1,942,500 1.23 0.65 1.90 St. 5 19 1,309,500 1.31 0.52 1.53 Middle St. 6 21 1,917,500 1.38 0.73 2.19 St. 7 16 3,411,500 0.98 0.64 1.71 St. 8 21 1,096,000 1.46 0.58 1.76 St. 9 20 1,623,750 1.30 0.65 1.92 St. 10 19 1,308,500 1.30 0.64 1.88 Western St. 11 20 911,250 1.35 0.65 1.91 St. 12 19 2,050,750 1.26 0.57 1.68 2018 St. 1 13 552,000 0.88 0.77 1.60 Eastern St. 2 16 653,000 1.19 0.67 1.87 St. 3 13 523,750 0.89 0.78 1.74 St. 4 18 1,042,750 1.21 0.65 1.82 St. 5 15 1,733,250 1.00 0.56 1.52 Middle St. 6 15 1,179,500 1.01 0.60 1.64 St. 7 16 2,318,500 1.02 0.54 1.48 St. 8 17 1,517,500 1.10 0.61 1.70 St. 9 15 2,379,500 0.94 0.48 1.26 St. 10 15 1,850,500 0.99 0.41 1.12 Western St. 11 15 303,000 1.10 0.64 1.71 St. 12 11 672,000 0.74 0.53 1.15 2019 St. 1 13 673,500 0.95 0.61 1.45 Eastern St. 2 16 355,750 1.18 0.71 1.76 St. 3 14 328,000 1.07 0.53 1.40 St. 4 23 1,224,500 1.65 0.57 1.79 St. 5 19 555,500 1.41 0.71 2.07 Middle St. 6 19 890,000 1.36 0.64 1.86 St. 7 19 1,371,000 1.32 0.73 2.14 St. 8 19 694,000 1.38 0.62 1.81 St. 9 26 2,524,000 1.77 0.53 1.73 St. 10 24 1,989,000 1.62 0.54 1.71 Western St. 11 23 2,651,500 1.57 0.59 1.81 St. 12 20 1,560,000 1.40 0.70 1.94 Diversity 2021, 13, 268 16 of 23 Diversity 2021, 13, x FOR PEER REVIEW 16 of 23

FigureFigure 2.2.Dendrogram Dendrogram representingrepresenting the similarity betw betweeneen Lake Burullus Burullus survey surveyeded stations stations during during yearsyears ( A(A)) 2017, 2017, ((BB)) 2018,2018, andand ((CC)) 2019.2019.

Diversity 2021, 13, 268 17 of 23 Diversity 2021, 13, x FOR PEER REVIEW 17 of 23

3 FigureFigure 3. Seasonal3. Seasonal mean mean of of zooplankton zooplankton densities densities (ind. (ind. mm3 ±± standardstandard deviation) deviation) in in Burullus Burullus Lake Lake by by taxonomic taxonomic division division in various basins (A) eastern basin, (B) middle basin, and (C) western basin. in various basins (A) eastern basin, (B) middle basin, and (C) western basin. Table 10. Seasonal average of zooplankton densities (ind./m3 ± standard deviation) and distribution in Burullus Lake by 3 Tabletaxonomic 10. Seasonal division average in various of zooplankton basins. densities (ind./m ± standard deviation) and distribution in Burullus Lake by taxonomic division in various basins. Basin Year Season Protozoa Rotifera Copepoda Cladocera Others Mean Basin YearWinter Season 10,667 Protozoa 1,170,667 Rotifera 158,000 Copepoda Cladocera 10667 102,667 Others 290533 Mean SpringWinter 3667 10,667 724,667 1,170,667 66000 158,000 2667 10,667 102,667 9333 161267 290,533

2017 Summer 0 358,667 164,333 4667 14,000 108333 Spring 3667 724,667 66,000 2667 9333 161,267 Autumn 7333 1,422,000 186,667 6000 41,333 332667

2017 Summer 0 358,667 164,333 4667 14,000 108,333 Winter 28,667 561,333 98,667 2667 41,333 146533 SpringAutumn 16,000 7333 7000 1,422,000 4667 186,667 6000 0 41,333 7333 7000 332,667 Eastern Basin Eastern Basin 2018 SummerWinter 1333 28,667 245,333 561,333 284,000 98,667 49,333 2667 14,66741,333 118933 146,533 AutumnSpring 40,000 16,000 788,667 7000 92,667 4667 12,000 0 93337333 188533 7000 Eastern Basin

20 19 Winter 18,000 138,000 23,667 2000 2667 36867 2018 Summer 1333 245,333 284,000 49,333 14,667 118,933 Autumn 40,000 788,667 92,667 12,000 9333 188,533

Diversity 2021, 13, 268 18 of 23

Table 10. Cont.

Basin Year Season Protozoa Rotifera Copepoda Cladocera Others Mean Winter 18,000 138,000 23,667 2000 2667 36,867 Spring 39,333 254,667 19,333 2667 5333 64,267

2019 Summer 0 300,667 269,333 690,667 1333 252,400 Autumn 6000 26,667 7333 667 1333 8400 Winter 27,400 1,664,400 282,800 15,600 4200 398,880 Spring 0 988,400 264,000 176,000 4400 286,560

2017 Summer 2800 1,323,600 154,000 29,200 9200 303,760 Autumn 4800 2,248,000 419,200 113,200 10,400 559,120 Winter 6400 1,525,200 114,000 4000 9200 331,760 Spring 0 1,000,000 70,200 32,200 2800 221,040

2018 Summer 7200 990,800 265,600 20,000 2400 257,200

Middle Basin Autumn 14,000 1,540,000 101,600 206,000 1200 372,560 Winter 40,600 164,600 75,600 58,800 8800 69,680 Spring 95,200 1,250,400 195,600 12,400 16,000 313,920

2019 Summer 13,600 1,424,800 142,400 121,600 5200 341,520 Autumn 6000 134,800 17,600 2800 1200 32,480 Winter 14,250 1,561,500 646,750 3500 2500 445,700 Spring 4000 618,000 210,000 36,000 6000 174,800

2017 Summer 2000 982,000 288,000 2500 4000 255,700 Autumn 12,750 1,229,250 258,500 3000 9750 302,650 Winter 4000 2,607,500 233,000 0 2500 569,400 Spring 1000 490,000 36,500 3000 0 106,100

2018 Summer 10,500 936,500 218,500 0 2000 233,500

Western Basin Autumn 6000 818,000 25,000 1000 1000 170,200 Winter 74,500 5,109,500 592,500 0 16,500 1,158,600 Spring 19,500 1,046,000 93,000 3000 74,500 247,200

2019 Summer 11,500 1,150,500 97,000 7500 5500 254,400 Autumn 10,000 355,000 46,500 9000 3000 84,700

Velliger of lamellibranch showed correlations with DO, NO2, PO4, Cu, and Zn (r = 1, 0.96, −0.88, 0.89, and −0.975, respectively). Salinity has negative correlations with Chlor-a and Cr (r = −1 and −0.925, respectively). The variations in correlation coefficients between salinity and zooplankton groups are due to the difference in species. The variations of mean salinity of the lake water are a result of the amount of drain water entering the lake from the southern part (this part receives freshwater supply from six drains) and seawater inflow to the lake from the northern part through El-Boughaz as well as the amount of evaporation from the external area of the lake. Salinity can be considered as a limiting factor for the abundance and diversity of zooplankton populations in the lake and the reverse relation between salinity and zooplankton. The pH concentration lies on the alkaline side, the minimum value recorded in the western sector showing an inverse relation to zooplankton. El-Enany [79] stated that Protozoa, Cladocera, and Copepoda were abundant in the stations characterized by high TS, EC, PO4, and Ca. The high numbers of drains from the River Nile, which carries high amounts of nutrients and salts, lead to the eutrophication of water. Diversity 2021, 13, 268 19 of 23

3.9. Comparison of Burullus Lake with Other lakes In current study, the physicochemical parameter values obtained from the Burullus Lake, in comparison to the most similar lakes in Egypt and the Mediterranean area, are presented in Table 11.

Table 11. Comparison between the physicochemical parameters values of Burullus Lake and the most similar lakes in Egypt and the Mediterranean area.

Marmara Lake Burullus Manzala Idku Mariout Tunisian Gölba¸sı(Hatay) (Manisa) Country Egypt Egypt Egypt Egypt Tunisia Turkey Turkey Temp(ºC) 21.77 15.3 22.3 24.2 19.7 21.8 19.8 Salinity‰ 4.6 15.6 3.3 4.07 0.2 15 pH 8.09 8.7 8.4 8.15 8.49 7.52 7.9 DO(mg L−1) 8.83 9.2 4.1 9.07 8.7 5.94 6.8 −1 NO3(mg L ) 0.283 0.37 0.16 0.72 16.35 −1 NO2(mg L ) 126.95 0.18 0.088 0.07 0.59 −1 NH4(mg L ) 0.61 0.05 4.5 5.25 0.58 0.61 TP(mg L−1) 0.64 0.2 0.7 0.42 0.18 0.22 COD(mg L−1) 100.39 48 42.5 BOD(mg L−1) 23.63 12.6 19.4 Chlo-a(mg L−1) 62.93 163 70.32 6.03 References This study [26][40][77][80][81][11]

4. Conclusions Lake Burullus is a very important lake in Egypt, due to its dimensions and economic activities. Burullus Lake is suffering from a high level of aquatic plants, expansion in fish farming, fishing, growing of human activities, and agricultural drainage effluents. In the current study, the properties of water quality, eutrophication, and zooplankton community of Burullus Lake were estimated based on three years (2017/2019) of seasonal monitoring at 12 stations. It could be concluded that water quality parameters showed wide variations, due to the discharge of drainage water from various pollution sources through different times and locations. The increase in pollution level may be due to the inflow of untreated water from industries and households around the drains of the lake, while the recorded increase in the eutrophication level may be attributed to the inflow of effluent of agricultural water with high nutrient levels. The heavy metal distribution in the lake depends on some factors, as characteristics, amounts, and type of input water. The current work is an attempt to examine the applicability of Carlson’s indices and trophic state indices for ranging the eutrophication case of Burullus Lake in concert with a numeral of physicochemical descriptors, as described previously. On the other hand, zooplankton species in Burullus Lake preferred a freshwater habitat than a marine habitat. The current study concluded that zooplankton are composed of four main groups: , , Protozoa, and Cladocera, in addition to rare groups, namely, Ostracoda, Nematoda, Annelid, Cirripeda, and Decapoda. During the period from 2017 to 2019, it observed about 98 zooplankton species in addition to six larval stages. Assessment of correlation matrix was carried out to check the significant relationship between biological and physicochemical factors. It is highly recommended that drainage water should be treated before reaching the lake, removing unwanted plants from the water bodies and providing decision-makers with data. Diversity 2021, 13, 268 20 of 23

Author Contributions: Conceptualization, A.E.A., A.M.M.H., A.M.S. and M.A.; methodology, A.E.A., A.M.M.H., A.M.S. and A.T.M.; software, A.E.A., A.M.M.H., M.A. and A.G.; formal analysis, A.E.A. and A.T.M.; investigation, A.M.M.H. and A.T.M.; resources, A.M.S., W.F.A. and A.G.; data cura- tion, A.M.S. and M.A.; writing—original draft preparation, A.E.A., A.M.M.H., W.F.A. and A.G.; writing—review and editing, A.E.A, M.A. and A.T.M.; visualization, A.E.A., A.T.M., W.F.A. and A.G.; supervision, A.M.M.H., A.M.S. and M.A.; project administration, A.E.A.; funding acquisition, A.T.M. and W.F.A. All authors have read and agreed to the published version of the manuscript. Funding: This research was funded by Taif University Researchers Supporting Project number TURSP-2020/39, Taif University, Taif, Saudi Arabia. Institutional Review Board Statement: Not applicable. Informed Consent Statement: Not applicable. Data Availability Statement: The data presented in this study are available in article. Acknowledgments: The authors gratefully acknowledge Taif University Researchers Supporting Project number TURSP-2020/39, Taif University, Taif, Saudi Arabia. Conflicts of Interest: The authors declare no conflict of interest.

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